Bat inventory in a Caatinga area in Northeastern Brazil , with a new occurrence in the state of Paraíba

The Caatinga is a semi-arid ecosystem with a long history of anthropic impacts and scientific negligence. Since bats are the second most diverse group of mammals and have wide ecological roles, a well-based comprehension of their diversity for an area is important for management and conservationist actions. The goal of this study is to provide a list of the bat species found in Private Reserve of Natural Heritage Fazenda Almas, Paraíba, Northeastern Brazil. By sampling with mist nets and exploring roosts, we captured 126 specimens and recorded 19 species from 5 families. The most abundant species were Artibeus planirostris, Peropteryx macrotis, Myotis nigricans, and Carollia perspicillata. We registered high diversity of Phyllostominae, as well as the occurrence of the genus Histiotus in the state for the first time. Our results indicate that Caatinga areas can maintain bat assemblages with levels of diversity similar to moist tropical areas, which highlights the need to expand the network of protected areas in this threatened ecosystem.


Introduction
Caatinga is a Neotropical ecosystem characterized by its accentuated seasonal weather, with scarce and irregular rainfall and high temperatures (Leal et al., 2005;Menezes et al., 2012).The vegetation includes arboreal and scrub forests with low canopy and with many xerophytic adaptations (Magalhães et al., 2013;Oliveira et al., 2012).It is one of the less protected ecosystems in Brazil, and one of the most threatened due to hundreds of years under unsustainable exploitation of its natural resources, now facing a process of desertification (Andrade et al., 2005;Velloso et al., 2002).The deficit of studies on its biodiversity and natural history represent a problem that is aggravated due to its history of widespread anthropic impact (Cruz et al., 2005).Recent studies show that the region is highly diverse with a considerable rate of endemic species (Sá-Neto and Marinho-Filho, 2013).However, the region as a whole is deficient of studies when compared with other Neotropical ecosystems (Santos et al., 2011).Regarding bats, inventories for the Caatinga are very scarce, and most of them were done more than five years ago (e.g.: Fabián, 2008;Sbragia and Cardoso, 2008;Gregorin et al., 2008;Astúa and Guerra, 2008;Nogueira et al., 2008;Rios et al., 2008;Sá-Neto and Marinho-Filho, 2013).The discovery of the most recently described bat genus (Xeronycteris) on the Caatinga (Gregorin and Ditchfield, 2005;Nogueira et al., 2014) might be a hint that there is a promising field for research on this Brazilian semi-arid ecosystem.Species inventories are important to support decision-making and planning on conservancy initiatives (Soulé and Kohm, 1989).In addition, a wellbased comprehension specifically about bat fauna on a region is important for conservation and management actions, since bats are the second most diverse group of mammals, with over 160 species registered in Brazil (Reis et al., 2007).Besides, they play important ecological roles, such as pollination, seed dispersal and population control for insects (Peracchi et al., 2006).Bats are also considered excellent bioindicators, since they respond to many environmental changes, and have responses associated to other taxa (Meyer et al., 2010).
Here we report results of the first bat survey conducted in the Private Reserve of Natural Heritage (RPPN) Fazenda Almas, located in the eastern Caatinga, in the state of Paraíba, northeastern Brazil.The region (Borborema geographical mesoregion) is under intense human occupation and traditional agribusiness exploitation (especially livestock), causing fast landscape modification and habitat loss, and making all efforts to study the regional biodiversity urgent.

Materials and methods
The present work was conducted in the Private Natural Heritage Reserve (RPPN) Fazenda Almas (7°28'19" S and 36°53'40" W), located between São José dos Cordeiros and Sumé (Barbosa et al., 2007), at about 650 m a.s.l., in mid-eastern Paraíba, in the northeastern of Brazil.The RPPN Fazenda Almas has an area of approximately 3,505 hectares.The native vegetation is represented by areas of arboreal Caatinga (dense and sparse) and "lajedos" (lithic outcrops typical of the Caatinga physiognomy with peculiar flora).Rainfall ranges between 500 and 800 mm/year, some years reaching as low as 350 mm, and temperature ranging between 26°C and 30°C (Araújo et al., 2011).

Data collection and analysis
We sampled at night during the months of September and November 2009 and during March and May 2010 using mist nets at ground level.
The nets were placed in pre-existent trails considered to be flyways (Kunz and Kurta, 1988;Flaquer et al., 2007), near trees bearing fruits and flowers, as well as water streams and structures (i.e., hollow trees, built structures) that are potential roosts.We did complementary samplings on roosts to capture species not commonly sampled using mist nets; roost-samplings took place during the day, using handnets.Sampling effort was calculated according to Straube and Bianconi (2002) as follows: Where E a represents the sample effort, A m the mist net area, N r the number of nets employed, H n hours per night, and N n the number of sampled nights.Collected bats were taken to the lab as voucher specimens.Taxonomical identification followed Gardner (2007), Gregorin andTaddei (2002), Vizotto andTaddei (1973).Specimens were preserved either in alcohol 70% after fixation by formalin 10% or taxidermied.We did the samplings under authorization n° 20321-2 (Ministério do Meio Ambiente).All specimens are deposited in Laboratório de Mamíferos' collection, at Federal University of Paraíba (UFPB 6013-6015 and UFPB 6111-6233).The diversity estimator Chao 1 (Chao, 1984) was calculated using EstimateS (Colwell, 2009), using only mist net data.A randomized species accumulation curve, with 95% confidence was calculated, using 1,000 random samplings with no reposition.

Results
The sampling effort totalized 3,663.6 m²/h.We captured 126 individuals, belonging to 19 species of five families (Table 1): Phyllostomidae (11 species), Vespertilionidae (4), Molossidae (2), Emballonuridae (1), and Noctilionidae (1).Artibeus planirostris (Spix, 1823) was the most abundant species, with 43 individuals (34.1%), followed that most of the areas studied on Caatinga are under-sampled, the distribution of sampled sites is inadequate, and there are extensive areas with no performed surveys, where a diversity even higher than the currently known one should be expected (Oliveira et al., 2003;Feijó and Lannguth, 2011).The bat fauna composition in the RPPN Fazenda Almas presents a typical tropical pattern, with the predominance of insectivorous, frugivorous and nectar-feeding species.This is commonly observed when the samplings are held using ground-level mist nets (Passos et al., 2003).Mist nets are the main sampling method used to conduct surveys in Brazil (Bergallo et al., 2003;Esbérard and Bergallo, 2005).The family Phyllos-

Discussion
This study represents the first bat inventory performed in the altitude of the dry region of Cariri, in the Paraíba State, northeastern Brazil.Comparing to other studies performed in the state, the RPPN Fazenda Almas has a richness similar to the study of Cruz et al. (2005), in another dry Caatinga area (20 species).However, bat diversity in the study area was higher than the ones by Percequillo et al. (2007) in an Atlantic forest area and Sousa et al. (2003) in a Caatinga enclave moist forest or "brejo de altitude" (13 species each).This support the thesis that the semi-arid Caatinga has a rich mammal fauna (Sá-Neto and Marinho-Filho, 2013).Considering tomidae is frequently the most representative in studies conducted this way, since a considerable number of species occur in sympatry and the family is the most diverse in the Neotropical region (Simmons, 2005;Wetterer et al., 2000;Gardner, 2007).
The species richness of the subfamily Phyllostominae registered in the study area is unusually high comparing to other surveys conducted in Caatinga (Cruz et al., 2005).This high species richness might be related to areas with low degree of environmental degradation, as the Phyllostominae are considered highly sensitive to vegetation covering alterations (Medellín et al., 2000), although the use of Neotropical bats as environmental indicator must follow a series of precautions (Cunto and Bernard, 2012).This information shows the importance and effectiveness of conservationist actions on the Caatinga biome, as well as reinforces the importance of the private party participation on the efforts, as the RPPN proves to be an effective alternative to increase the number of protected areas.
The dominance of Artibeus planirostris (34.1% of total captures) is unusual for Caatinga inventories, contrasting sharply to data from Sbragia and Cardoso (2008), Silva et al. (2001) and Silva et al. (2004) who registered low abundance of this species in sites at Ceará.Gregorin et al. (2008)  The individuals of Micronycteris megalotis had morphological traits that fit in M. microtis Miller, 1898 description as well.The diagnostic trait proposed by Simmons (1996) upon the species description is the length of the hairs from the inner edge of the ear (3 mm for M. microtis, 7-8 mm for M. megalotis).Siles et al. (2013) points the taxonomic problems between the two species of Micronycteris, as well as problems setting the boundaries between other species within the genus.
The validity of Micronycteris microtis can be questioned due to conflicting data (Porter et al., 2007).The incongruence between the field data and the literature, and the superposition of diagnostic traits might indicate the necessity of a revision of the genus (Ecsobedo-Cabrera et al., 2006;Ribas et al., 2013).We support the adoption of M. megalotis as it is also the taxon recognized for the longest time (Alonso-Mejía and Medellín, 1991).
The captured individuals of Histiotus sp. were similar to Histiotus velatus (I.Geoffroy, 1824).However, the specimens registered in the study area present unique ear morphology with light dorsal hair that distinguishes them from the typical H. velatus.
The present work has also first registered the occurrence of the genus Histiotus to the state, extending the genus distribution by 195 km northeast.The distance from the nearest record and the study area indicates a still deficient knowledge, and points out the importance of more extensive surveys and biogeography studies both as a gap-closing effort and as a way to unveil the genus' distribution on the Brazilian semi-arid regions.

ReferencesFigure 1 .
Figure 1.Species' accumulation curve of bat species sampled using mist nets at RPPN Fazenda Almas, northeastern Brazil, from August 2009 to May 2010, with the results of Chao 1 estimator.Full line represents the average observed number of species, and dotted lines represent the upper and lower 95% confidence interval.

Table 1 .
List of Species sampled at RPPN Fazenda Almas, in the northeastern ofBrazil, from August 2009 to May 2010, discriminatedbetween roost and mist net captures.Conservation status according toChiarello et al. (2004), where DD stands for Data Deficient and NA stands for Not Available.Percentage of the species' contribution to all captures is discriminated between mist net captures, roost samplings and total samplings.